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Sequential process of solid-state cultivation with fungal consortium and ethanol fermentation by Saccharomyces cerevisiae from sugarcane bagasse

Abstract

Solid-state cultivation (SSC) is the microbial growth on solid supports, producing a nutrient-rich solution by cell enzymes that may be further used as a generic microbial medium. “Second-generation” ethanol is obtained by fermentation from mainly the acid hydrolysates of lignocellulosic wastes, generating several microbial growth inhibitors. Thus, this research aimed at evaluating the feasibility of ethanol fermentation from sugarcane bagasse hydrolysate after SSC with vinasse as the impregnating solution by a consortium of A. niger and T. reesei as opposed to the conventional method of acid hydrolysis. Fermentation of the hydrolysate from SSC leading to the yield of 0.40 g g−1, i.e., about 78% of maximum stoichiometric indicating that the nonconventional process allowed the use of two by-products from sugarcane processing in addition to ethanol production from glucose release.

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References

  1. Codato CB, Martini C, Ceccato-Antonini SR, Bastos RG (2018) Ethanol production from Dekkera bruxellensis in synthetic media with pentose. Braz J Chem Eng 35:11–17. https://doi.org/10.1590/0104-6632.20180351s20160475

    CAS  Article  Google Scholar 

  2. Barcelos CA, Maeda RN, Betancur GJV, Pereira JRN (2013) The essentialness of delignification on enzymatic hydrolysis of sugarcane bagasse cellulignin for second generation ethanol production. Waste Biomass Valorization 4:341–346. https://doi.org/10.1007/s12649-012-9137-3

    CAS  Article  Google Scholar 

  3. Martini C, Tauk-Tornisielo SM, Codato CB, Basto RG, Ceccato-Antonini SR (2016) A strain of Meyerozyma guilliermondii isolated from sugarcane juice able to grow and ferment pentoses in synthetic and bagasse hydrolysates media. World J Microbiol Biotechnol 32:1–9. https://doi.org/10.1007/s11274-016-2036-1

    CAS  Article  Google Scholar 

  4. Khonngam T, Salakkam A (2019) Bioconversion of sugarcane bagasse and dry spent yeast to ethanol through a sequential process consisting of solid-state fermentation, hydrolysis, and submerged fermentation. Biochem Eng J 150:107284. https://doi.org/10.1016/j.bej.2019.107284

    CAS  Article  Google Scholar 

  5. Prajapati BP, Jana UK, Suryawanshi RK, Kango N (2020) Sugarcane bagasse saccharification using Aspergillus tubingensis enzymatic cocktail for 2G bio-ethanol production. Renew Energy 152:653–663. https://doi.org/10.1016/j.renene.2020.01.063

    CAS  Article  Google Scholar 

  6. Langan P, Petridis LO’, Neill HM, Pingali SV, Foston M, Yoshiharu N, Schulz R, Lindner B, Hanson BL, Harton S, Heller WT, Urban V, Evans BR, Gnanakaran S, Ragauskas AJ, Smith JC, Davison B (2014) Common processes drive the thermochemical pretreatment of lignocellulosic biomass. Green Chem 16:63–68. https://doi.org/10.1039/C3GC41962B

    CAS  Article  Google Scholar 

  7. Sun Y, Cheng J (2005) Dilute acid pretreatment of rye straw and bermudagrass for ethanol production. Bioresource Technol 96:1599–1606. https://doi.org/10.1016/j.biortech.2004.12.022

    CAS  Article  Google Scholar 

  8. Taherzadeh MJ, Karimi K (2008) Pretreatment of lignocellulosic wastes to improve ethanol and biogas production: a review. Int J Mol Sci 9:1621–1651

    CAS  Article  Google Scholar 

  9. Kumar R, Mago G, Balan V, Wyman CE (2009) Physical and chemical characterizations of corn stover and poplar solids resulting from leading pretreatment technologies. Bioresource Technol 100:3948–3962. https://doi.org/10.1016/j.biortech.2009.01.075

    CAS  Article  Google Scholar 

  10. Yan X, Wang Z, Zhang K, Si M, Liu M, Chai L, Liu X, Shi Y (2017) Bacteria-enhanced dilute acid pretreatment of lignocellulosic biomass. Bioresource Technol 245:419–425. https://doi.org/10.1016/j.biortech.2017.08.037

    CAS  Article  Google Scholar 

  11. Solarte-Toro J, Romero-Gacrcía JM, Martínez-Patiño JC, Ruiz-Ramos E, Castro-Galiano E, Cardona-Alzate CA (2019) Acid pretreatment of lignocellulosic biomass for energy vectors production: a review focused on operational conditions and techno-economic assessment for bioethanol production . Renewable Sustainable Energy Rev 107:587–601. https://doi.org/10.1016/j.rser.2019.02.024

    CAS  Article  Google Scholar 

  12. Soares PA, Vaz-Rossel CE (2007) Conversão de celulose pela tecnologia organosolv, vol 3. NAIPPE-USP, São Paulo

    Google Scholar 

  13. Olsson L, Hahn-Hägerdal B (2000) Fermentation of lignocellulosic hydrolysates II: inhibitors and mechanisms of inhibition. Bioresource Technol 74:25–33. https://doi.org/10.1016/S0960-8524(99)00161-3

    Article  Google Scholar 

  14. Hahn-Hägerdal B, Karhumaa K, Fonseca C, Spencer-Martins I, Gorwa-Grauslund M (2007) Towards industrial pentose-fermenting yeast strains. Appl Microbiol Biotechnol 74:937–953. https://doi.org/10.1007/s00253-006-0827-2

    CAS  Article  PubMed  Google Scholar 

  15. Fonseca BG, Moutta RO, Ferraz FO, Vieira ER, Nogueira AS, Baratella BF, Rodrigues LC, Hou-Rui Z, da Silva SS (2011) Biological detoxification of different hemicellulosic hydrolysates using Issatchenkia occidentalis CCTCC M 206097. J Ind Microbiol Biotechnol 38:199–207. https://doi.org/10.1007/s10295-010-0845-z

    CAS  Article  PubMed  Google Scholar 

  16. Khajeeram S, Unrean P (2017) Techno economic assessment of high solid simultaneous saccharification and fermentation and economic impacts of yeast consortium and on-site enzyme production technologies. Energy 122:194–203. https://doi.org/10.1016/j.energy.2017.01.090

    CAS  Article  Google Scholar 

  17. Gutierrez-Correa M, Tengerdy RP (1997) Production of cellulase on sugar cane bagasse by fungal mixed culture solid substrate fermentation. Biotechnol Lett 19:665–667. https://doi.org/10.1023/A:1018342916095

    CAS  Article  Google Scholar 

  18. Pandey A (2003) Solid-state fermentation. Biochem Eng J 13:81–84. https://doi.org/10.1016/S1369-703X(02)00121-3

    CAS  Article  Google Scholar 

  19. Thomas L, Larroche C, Pandey A (2013) Current developments in solid-state fermentation. Biochem Eng J 81:146–161. https://doi.org/10.1016/j.bej.2013.10.013

    CAS  Article  Google Scholar 

  20. Gutiérrez-Correa M, Villena GK (2017) Batch and repeated batch cellulase production by mixed cultures of Trichoderma reesei and Aspergillus niger or Aspergillus phoenicis. J Microbiol Biotechnol Res 2(6):929–935

    Google Scholar 

  21. Campanhol BS, Silveira GC, Castro MC, Ceccato-Antonini SR, Bastos RG (2019) Effect of the nutrient solution in the microbial production of citric acid from sugarcane bagasse and vinasse. Biocatal Agric Biotechnol 19:101147. https://doi.org/10.1016/j.bcab.2019.101147

    Article  Google Scholar 

  22. Bastos RG, França HCR, Campanhol BS, Castro MC, Silveira GC (2017). Sequential process of citric acid production in sugarcane bagasse by microbial consortium and ethanol fermentation from fungal extract. In: 2017 ASABE Annual International Meeting, Spokane, WA. Proceedings ASABE 2017 1700161. https://doi.org/10.13031/aim.201700161

  23. Salakkam A, Kingpho Y, Najunhom S, Aiamsonthi K, Kaewlao S, Reungsang A (2017) Bioconversion of soybean residue for use as alternative nutrient source for ethanol fermentation. Biochem Eng J 125:65–72. https://doi.org/10.1016/j.bej.2017.05.020

    CAS  Article  Google Scholar 

  24. Kumar D, Jain VK, Shanker G, Srivastava A (2003) Citric acid production by solid state fermentation using sugarcane bagasse. Process Biochem 38:1731–1738. https://doi.org/10.1016/S0032-9592(02)00252-2

    CAS  Article  Google Scholar 

  25. Oliveira AF, Matos VC, Bastos RG (2012) Cultivation of Aspergillus niger on sugarcane bagasse with vinasse. Biosci J 28:889–894

    Google Scholar 

  26. Bastos RG, Morais DV, Volpi MPC (2015) Influence of solid moisture and bed height on cultivation of Aspergillus niger from sugarcane bagasse with vinasse. Braz J Chem Eng 32:377–384. https://doi.org/10.1590/0104-6632.20150322s00003423

    Article  Google Scholar 

  27. Federation WE, APH Association (2005) Standard methods for the examination of water and wastewater. American Public Health Association (APHA): Washington, DC, p 1220

  28. Motta FL, Santana MHA (2014) Solid-state fermentation for humic acids production by a Trichoderma reesei strain using an oil palm empty fruit bunch as the substrate. Appl Biochem Biotechnol 172:2205–2217. https://doi.org/10.1007/s12010-013-0668-2

    CAS  Article  PubMed  Google Scholar 

  29. Khosravi-Darani K, Zoghi A (2008) Comparison of pretreatment strategies of sugarcane bagasse experimental design for citric acid production. Bioresource Technol 99:6986–6993. https://doi.org/10.1016/j.biortech.2008.01.024

    CAS  Article  Google Scholar 

  30. Bastos RG, Motta FL, Santana MHA (2016) Oxygen transfer in the solid-state cultivation of D. monoceras on polyurethane foam as an inert support. Braz J Chem Eng 33:793–799. https://doi.org/10.1590/0104-6632.20160334s20150262

    CAS  Article  Google Scholar 

  31. Ferrari FA, Motta FL, Bastos RG, Santana MHA (2013) The solid state cultivation of Streptococcus zooepidemicus in polyurethane foam as a strategy for the production of hyaluronic acid. Appl Biochem Biotechnol 170:1491–1502. https://doi.org/10.1007/s12010-013-0293-0

    CAS  Article  PubMed  Google Scholar 

  32. Silva JPA, Carneiro LM, Conceição IR (2014) Assessment of advanced oxidative processes based on heterogeneous catalysis as a detoxification method of rice straw hemicellulose hydrolysate and their effect on ethanol production by Pichia stipites. Biomass Convers Biorefinery 4:225–236. https://doi.org/10.1007/s13399-013-0104-4

    CAS  Article  Google Scholar 

  33. Mekala NK, Singhania RR, Sukumaran RK, Pandey A (2008) Cellulase production under solidstate fermentation by Trichoderma reesei RUT C30 Statistical optimization of process parameters. Appl Biochem Biotechnol 151:122–131. https://doi.org/10.1007/s12010-008-8156-9

    CAS  Article  PubMed  Google Scholar 

  34. Maeda RN, Serpa VI, Rocha VAL, Mesquita RAA, Anna LMMS, Castro AM, Driemeier CE, Pereira-Junior N, Polikarpov I (2011) Enzymatic hydrolysis of pretreated sugar cane bagasse using Penicillium funiculosum and Trichoderma harzianum cellulases. Process Biochem 46:1196–1201. https://doi.org/10.1016/j.procbio.2011.01.022

    CAS  Article  Google Scholar 

  35. Rodríguez-Zúñiga UF, Neto VB, Couri S, Crestana S, Farinas CS (2014) Use of spectroscopic and imaging techniques to evaluate pretreatment sugarcane bagasse as a substrate for cellulase production under solid-state fermentation. Appl Biochem Biotechnol 172(5):2348–2362

    Article  Google Scholar 

  36. Sørensen A, Andersen JJ, Ahring BK, Teller PJ, Lübeck M (2014) Screening of carbon sources for beta-glucosidase production by Aspergillus saccharolyticus. Int Biodeterior Biodegrad 93:78–83. https://doi.org/10.1016/j.ibiod.2014.05.011

    CAS  Article  Google Scholar 

  37. Rocha NRDAF, Martin C, Soares IB, Maior AMS, Baudel HM, Abreu CAM (2011) Dilute mixed-acid pretreatment of sugarcane bagasse for ethanol production. Biomass Bioenerg 35(1):663–670. https://doi.org/10.1016/j.biombioe.2010.10.018

    CAS  Article  Google Scholar 

  38. Rodrigues RCLB, Rocha GJM, Rodrigues-Junior D, Filho HJI, Felipe MDGA (2010) Scale-up of diluted sulfuric acid hydrolysis for producing sugarcane bagasse hemicellulosic hydrolisate (SBHH). Bioresource Technol 101:1247–1253. https://doi.org/10.1016/j.biortech.2009.09.034

    CAS  Article  Google Scholar 

  39. Della-Bianca BE, Hulster E, Pronk JT, van Maris AJA, Gombert AK (2014) Physiology of the fuel ethanol strain Saccharomyces cerevisiae PE-2 at low pH indicates a context-dependent performance relevant for industrial applications. FEMS Yeast Res 14(8):1196–1205. https://doi.org/10.1111/1567-1364.12217

    CAS  Article  PubMed  Google Scholar 

  40. Dorta C, de Oliva-Neto P, Abreu-Neto MS, Nicolau-Junior N, Nagashima AI (2006) Synergism among lactic acid, sulfite, pH and ethanol in alcoholic fermentation of Saccharomyces cerevisiae (PE-2 and M-26). World J Microbiol Biotechnol 22:177–182. https://doi.org/10.1007/s11274-005-9016-1

    CAS  Article  Google Scholar 

  41. Blomqvist J, South E, Tiukova L, Momeni MH, Hansson H, Ståhlberg J, Horn SJ, Schnürer J, Passoth V (2011) Fermentation of lignocellulosic hydrolysate by the alternative industrial ethanol yeast Dekkera bruxellensis. Lett Appl Microbiol 53(1):73–78. https://doi.org/10.1111/j.1472-765X.2011.03067.x

    CAS  Article  PubMed  Google Scholar 

  42. Hahn-Hagerdal B, Linden T, Senac T, Skoog K (1991) Ethanolic fermentation of pentoses in lignocellulose hydrolysate. Appl Biochem Biotechnol 28:28–29. https://doi.org/10.1007/bf02922595

    Article  Google Scholar 

  43. Amartey S, Jeffries T (1996) An improvement in Pichia stipitis fermentation of acid-hydrolysed hemicellulose achieved by overliming (calcium hydroxide treatment) and strain adaptation. World J Microbiol Biotechnol 12:281–283. https://doi.org/10.1007/bf00360928

    CAS  Article  PubMed  Google Scholar 

  44. Awafo VA, Chahal DS, Simpson BK (1998) Optimization of ethanol production by Saccharomyces cerevisiae (ATCC 60868) and Pichia stipitis y-7124: a response surface model for simultaneous hydrolysis and fermentation of wheat straw. J Food Biochem 22:489–509. https://doi.org/10.1111/j.1745-4514.1998.tb00258.x

    CAS  Article  Google Scholar 

  45. Nigam JN (2001) Development of xylose-fermenting yeast Pichia stipitis for ethanol production through adaptation on hardwood hemicellulose acid prehydrolysate. J Appl Microbiol 90:208–215. https://doi.org/10.1046/j.1365-2672.2001.01234.x

    CAS  Article  PubMed  Google Scholar 

  46. Agbogbo FK, Cowaed-Kelly G, Torry-Smith M, Wenger K, Jeffries TW (2007) The effect of initial cell concentration on xylose fermentation by Pichia stipites. Appl Biochem Biotechnol. https://doi.org/10.1007/s12010-007-9086-7

    Article  PubMed  Google Scholar 

  47. Kuhar S, Nair LM, Kuhad RC (2008) Pretreatment of lignocellulosic material with fungi capable of higher lignin degradation and lower carbohydrate degradation improves substrate acid hydrolysis and the eventual conversion to ethanol. Can J Microbiol 54:305–313. https://doi.org/10.1139/w08-003

    CAS  Article  PubMed  Google Scholar 

  48. Ceccato-Antonini SR, Codato CB, Martini C, Bastos RG, Tauk-Tornisielo SM (2017) Yeast for pentose fermentation: isolation, screening, performance, manipulation and prospects. In: Buckeridge MSD, Souza AP (eds) Advances of basic science for second generation bioethanol from sugarcane. Springer, Switzerland, pp 133–157

    Chapter  Google Scholar 

  49. Canilha L, Carvalho W, Felipe MGA, Silva JBA, Giulietti M (2010) Ethanol production from sugarcane bagasse hydrolysate using Pichia stipitis. Appl Biochem Biotechnol 161:84–92. https://doi.org/10.1007/s12010-009-8792-8

    CAS  Article  PubMed  Google Scholar 

  50. Ximenes E, Kim Y, Mosier N, Dien B, Ladisch MR (2011) Deactivation of cellulases by phenols. Enzym Microb Technol 48:54–60. https://doi.org/10.1016/j.enzmictec.2010.09.006

    CAS  Article  Google Scholar 

  51. Michelin M, Ximenes E, Polizeli MLTM, Ladisch MR (2016) Effect of phenolic compounds from pretreated sugarcane bagasse on cellulolytic and hemicellulolytic activities. Bioresour Technol 199:275–278. https://doi.org/10.1016/j.biortech.2015.08.120

    CAS  Article  PubMed  Google Scholar 

  52. Cao G, Ximenes E, Nichols NN, Zhang L, Ladisch MR (2013) Biological abatement of cellulase inhibitors. Bioresour Technol 146:604–610. https://doi.org/10.1016/j.biortech.2013.07.112

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)—Brazil (Finance Code 88882.378479/2019-01 and 001).

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Correspondence to Reinaldo Gaspar Bastos.

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Brito Codato, C., Gaspar Bastos, R. & Ceccato-Antonini, S.R. Sequential process of solid-state cultivation with fungal consortium and ethanol fermentation by Saccharomyces cerevisiae from sugarcane bagasse. Bioprocess Biosyst Eng 44, 1–8 (2021). https://doi.org/10.1007/s00449-021-02588-6

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Keywords

  • Solid-state cultivation
  • 2G ethanol
  • Sugarcane bagasse
  • Acid hydrolysates
  • Vinasse